Pol. J. Environ. Stud. Vol. 29, No. 3 (2020), 2031-2040 DOI: 10.15244/pjoes/111509 ONLINE PUBLICATION DATE: 2020-03-16

Review The Future Prospects of Arbuscular Mycorrhizal Fungi in Slope Ecological Restoration

Yujie Yan1, 2, Bingqin Zhao2, Wennian Xu2 , Fei Yu1, 2, Wenjing Liu1, 2, Dong Xia2, 3*

1China Three Gorges University, College of Biological and Pharmaceutical Sciences Yichang, Hubei, China 2China Three Gorges University, Collaborative Innovation Center for Geo-Hazards and Eco-Environment in Three Gorges, Yichang, Hubei , China 3China Three Gorges University, Engineering Research Center of Eco-Environment in Three Gorges Reservoir, Yichang, Hubei , China

Received: 12 June 2019 Accepted: 4 August 2019

Abstract

The rapid development of transportation and urbanization has promoted the continuous innovation of slope ecological restoration technology (SERT). More environmentally friendly and efficient technologies are being developed and perfected to make the restored slopes sustainable and be able to integrate into the natural environment, in which microbial- remediation technology was been taken into account. Arbuscular mycorrhizal fungi (AMF), a microbial material commonly used in ecological restoration, has a symbiotic relationship with the majority of terrestrial to provide water and nutrients, and has been successfully used in the field of ecological restoration in recent years. Combining stress tolerance and growth promotion for plants with improvement of soils properties through strengthened associations with AMF would help to increase the efficiency of slope ecological restoration. This review mainly introduces AMF research progress in terms of plant stress tolerance, ecological optimization, and symbiosis with plant species for phytoremediation, summarizes the current challenges faced in the application of AMF in ecological restoration projects, and highlights the future research direction for resolving the mentioned problems. Finally, theoretical study and field applications are combined to provide an overview of the future application prospects in slope ecological restoration.

Keywords: arbuscular mycorrhiza, ecological restoration, slope engineering, stress tolerance

Introduction and making sustainable development choices [3-6]. As the basic unit of ecological damage The rapid development of transportation and caused by infrastructure construction, engineering urbanization not only provides convenience for human slopes directly affect the quality of the urban ecological beings but also is destroying the [1, 2]. environment [1, 3]. Slope ecological restoration, which Global attention has focused on restoring damaged aims at assimilating the slope ecological environment into the surrounding natural landscape [1, 2], is defined as an artificial restoration combining plant and non- living materials with civil engineering technology to *e-mail: [email protected] mitigate slope instability and erosion [3, 7, 8]. Existing 2032 Yan Y., et al. high-efficiency technologies usually adopt various the beginning of a rock greening project [8, 19, 21]. In strengthening facilities or bonding materials to the the intervening years, the soil-flock greening method substrate in order to establish a relatively stable slope [1, (1983) and the continuous fibers greening method 2, 9]. Nevertheless, long-term stability is still hard to be (1987), which synthesized the continuous reinforced satisfied entirely by a substantial proportion of existing geotechnical method proposed by Henri Vidal [22], were methods, thus microbial-phytoremediation technology is subsequently developed. At the end of the 20th century, considered for SERT under the demand of sustainable Japan developed the permanent greening method of soil development. microorganisms, which used soil microorganisms to Microbes with the ability to improve the nutrient accelerate the soil transformation of rocks, reflecting the transmission efficiency of plants and soil make the plant- important role of soil microorganisms in the process of microbial technology a global hotspot in the restoration slope ecological restoration [8, 23]. field [6, 10, 11]. Arbuscular mycorrhizal fungi (AMF), Research on substrate composition, species selection, the most widely distributed plant symbiotic fungi in construction technology and maintenance management nature, are one of the typical representatives [11, 12]. of SERT has entered a mature stage [3]. Existing Through the production of their two special structures, commonly used technologies can be classified according vesicles and arbuscules, AMF can provide effective to different habitat construction methods, including: assistance for interaction between plants and fungi by plant direct covering, planting hole construction, means of delivering soil nutrients to the hosts in return reinforced filling and spray sowing [8]. Throughout the for carbon [5, 10]. A significant amount of research history of SERT development, early technologies such has focused on the function of AMF in ecological as green geonet [24] and vegetated riprap [25] usually restoration, mainly the improvement of plant stress establish plant communities or construct planting holes tolerance [4, 13], soil conditions [12, 14, 15], and on the slope to create a better surrounding for plant community structure [4, 16, 17], indicating that AMF growth [24]. Though less construction technology was are efficient materials for ecological restoration. Though required by those methods, the long-term revegetation the application of AMF in the field of soil restoration effect cannot be guaranteed [8]. The later development has proliferated rapidly in recent years [12], efforts in of SERT combined mechanical reinforcement with mycorrhizal technology applied to SERT are relatively vegetation reconstruction [26], and added different types limited. of hard materials and environment-friendly materials [3, This review first summarizes the effects of AMF on 27], more consideration was paid to environmental and plant stress tolerance and slope ecological optimization biological needs while guaranteeing slope stability. in theory and then intends to introduce the symbiosis between AMF and pioneer species for phytoremediation The Challenges of SERT in order to ensure the feasibility of the application. Finally, actual problems in project applications are Along with increased requirements for innovative, presented in addition to advice and proposals on those green, coordinated and sustainable development, SERT problems to overview the future application prospects in is challenged with: how to improve the stress tolerance slope ecological restoration. of the slope system [28], how to strengthen slope safety [3, 26], and how to beautify landscaping, adding to the complexity of the implementation. Progress and Challenges of SERT The construction of infrastructure will create a large amount of excavation slope, disturb the original Specialization and the Development of SERT landform and vegetation, aggravate the deterioration of the ecological environment, and also form a hidden The earliest embryo of SERT was vegetation slope danger of geological disasters. Existing technologies protection initially used for bank revetment and barren often through the artificial addition of nutrients, or hills control [3, 8]. In the 1930s, SERT was first introduce pioneer plants [28], especially shrubs and introduced to Central Europe and has rapidly developed herbs with developed roots, strong expansibility and since then [8]. The spray seeding machine developed ecological functions adapted to local natural vegetation by an American company in the 1950s realized the communities in order to improve the stress tolerance mechanization of SERT [18], and the hydraulic seeding of the whole slope system [29], and through rational technology using emulsified asphalt as a binder was plant disposition for better landscaping. At the same invented in Britain. In the early 1960s, Japan promoted time, the slope safety factor is strengthened by the SERT on a large scale through continuous improvement construction of reinforcement facilities (reinforced and innovation based on the experience in Europe and filling methods), laying rock bolts, metal protective nets, America [19]. In the 1980s, while the three-dimensional or adding bonding materials (spray sowing methods) to grass planting technology was widely used in Western the substrate [3, 8, 27]. The series of artificial assistant countries [20], Japan developed the fiber-soil greening methods has consumed lots of effort yet the sustainability method, which is also the embryonic form of the of its development was still not guaranteed. Faced with thick-layer base material spraying method, marking these challenges, new technologies such as restoration The Future Prospects of Arbuscular Mycorrhizal... 2033 ecology, macromolecule materials and microbiology are combined with slope restoration technology to enhance the restoration effect [3, 8]. This paper will investigate the role of AMF in overcoming the challenges of SERT, and evaluate its feasibility and advantages.

AMF and Slope Environmental Stress

Benefits under Physical Stress

Restoration technique should be adjusted judging from different characteristics of the macro environment, climate characteristics, and other physical factors [7]. The features of these restoration projects, primarily long-distance, large area, and limited time, result in difficulties in conventional manual maintenance [1, 30]. Slopes located in arid and simiarid regions present more difficulties to management due to the low amount of species diversity and the fragile ecological environment brought by low rainfall [1, 7, 31]. Current technologies in arid areas focus on introducing high Fig. 2. Positive effects of arbuscular mycorrhizal colonization; drought-resistant species or improving the substrate the hyphal network (in purple) could extend beyond the formula by adding super absorbent composite to phosphate depletion zone (in grey) to access a better area for alleviate water shortage [1], yet those methods only phosphate absorption. worked effectively in a certain range of time [31, 32]. AMF can be utilized in restoration to improve plant tolerance under drought conditions because of the lower mobility) [10], and a lower proline, MDA, and improvement of plant water utilization efficiency of H2O2 content compared with the untreated samples AMF (Fig. 2) [4, 10, 33]. Previous researchers have under water deficit conditions [33, 34]. These results proven that plant drought tolerance is enhanced after provide strong evidence for improved conditions as a inoculation by detecting the growth and branching of result of AMF, both through the plant enzyme defense the root system and the activity of the defense system in system and osmotic regulatory network [33, 34]. plants (Fig. 1) [10, 33]. Seedlings inoculated with AMF Slopes located in more pluvial regions are affected had higher antioxidant enzyme (Tyagi et al. 2017) [34], by heavy rainfall and are frequently subjected to ascorbic acid, glutathione peroxidase [33], glomalin- damage caused by rain erosion [35]. Relevant capacities related soil (GRSP), soluble sugar contents [34], of AMF, for instance enhancing soil-reinforcement of nutrient uptake efficiency (especially nutrients with the root system and reducing leaching loss, are favorable

Fig. 1. Root system architectures of trifoliate orange seedlings inoculated (+AMF) with Glomus mosseae, not inoculated (−AMF), exposed to ample water (AW), or drought stress (DS). 2034 Yan Y., et al. for soil conservation [2, 5, 36]. There is evidence that Non-biodegradable metal materials used in restoration the negative impact of increased precipitation, the projects to play a reinforcing role would result in Zn or most typical example of which is nutrient losses, may iron (Fe) accumulation in soil as well [3]. Experiments be mitigated by AMF through their extensive hyphal proved that inoculation of AMF can promote the growth network [37, 38], and this function may even be of plants under heavy metal stress such as Cu [47], Pb improved under high rainfall intensity [37]. Unlike the [53], Zn [48], and Cd [54]. Although increased Cu supply stress of heavy rainfall on the whole soil microbial group will result in a significant decrease in the infection rate and bacterial abundance, AMF abundance increased and spore density of AMF due to the strong fungal after extreme rainfall [39], which provided evidence of toxicity of Cu [55], many experiments showed the the ability of AMF to maintain community stability. ability of AMF to promote plant growth – especially Very low temperatures and frozen damage will a significant increase in plant biomass and P uptake generate relatively large effects on the stability of the and immobilization of soil Cu by mycelia [10, 46]. substrate and are unfavorable for vegetation growth [40, In addition to help take up Zn from Zn-deficient soil, 41], making it difficult to conduct SERT in high altitude AMF can also protect plants against Zn toxicity under and cold regions. Good symbiotic relationships between high soil Zn concentrations [56]. This bi-directional AMF and certain plants under cold climate environment regulation may be attributed to a Zn threshold in soil, is able to improve the nutritional status of hosts [42] below which plant Zn nutrition can be improved, while and facilitate their growth [43, 44]. Such promotion above which mycorrhizal infection will decrease in may possibly be related to nitrate reductase activity [42] order to reduce Zn accumulation in plants [56]. In and the photosynthetic pigments contents [44], which conclusion, the roles of AMF inoculation under heavy are significantly higher in mycorrhiza than that in non- metal stress include the following: improved plant mycorrhizal roots. Surveys conducted on the Qinghai- growth [57]; improved (P) nutrition, which Tibet Plateau showed that a variety of AMF flora also may be related to the detoxification of polyphosphates to had colonization ability in cold-dominated regions [45], heavy metals [58]; and immobilization of heavy metals which made it possible to screen native AMF from high and secretion of chelates to reduce their toxicity and and cold regions and apply them in restoration projects bioavailability [46]. after multiplication. Resistance to Pathogenic Microbial Attack Adaptation to Slope Chemical Stress Due to neglect and infrequent maintenance, slope A high percentage of the construction materials in vegetation is often not treated promptly when attacked SERT is eventually deposited in the substrate, changing by exotic pathogens or pests. Although chemical agents the soil chemical properties, or interfering with nutrient have been sprayed on the damaged plants and might cycling between plants and soil. The application of appear to work in the short term, the costs of manual mycorrhizal technology to the restoration of chemical- labor, material and financial resources increase the contaminated soil is the focus of current AMF research difficulties associated with management; therefore, [46-48], and a reasonable scheme can be designed on the flexible methods still need to be developed. basis of advanced research results for slope ecological AMF can offer protection to host plants against restoration. various soil-borne pathogens and pests, either through In order to improve substrate stability, special changing plant activities or changing plant endogenous bonding materials have invariably been added [3], regulators (Fig. 2) [4, 13, 17, 59]. The antagonistic which may change the soil pH along with the continued relationships between AMF and herbivorous insects deposition of indecomposable chemical compositions and and parasites largely depend on the release of volatile have detrimental impact on the vegetation establishment organic compounds by hosts [59]. With respect to [49]. Two hypotheses explained the mechanism of the disease resistance, Wehner et al. [13] summarized the adaptation of AMF to soil pH: directly through the mechanism of AMF against pathogens as interference metabolic activities and secretions of hypha [46], or competition (direct interactions) and exploitation indirectly through changing the component of plant root competition (indirect interactions). Studies have also exudates [49, 50]. The preference of AMF for alkaline or shown that the interaction between different AMF neutral soil and the role of AMF in alleviating acidic soil combinations may play a good role in pathogen stress had also been proved by Ouzounidou et al. [49]. In protection [13]. Therefore, Wehner et al. [13] suggested addition, the absorption of alkaline earth metal elements shifting the focus from single to multiple species affected by AMF contributes to the rhizosphere pH of AMF assemblages and to take account of the change as well [51]. All these results proved the indirect functional groups that coexist with roots. Additionally, effect of AMF on soil pH regulation. the interaction between AMF and pathogens makes Evidence showed that elements that would result AMF have a certain effect on biological invasion [4, in excessive deposition of heavy metal elements on 12], which can be applied to protect slope plants from slopes, originate mainly from highway traffic [52], rock invasive species, maintaining the overall beauty of slope weathering [53], and corrosion of metal materials [52]. vegetation. The Future Prospects of Arbuscular Mycorrhizal... 2035

Optimization of the Slope Ecological Effects on Plant Growth and Development Environment The promotion of plant nutrient uptake by AMF has Soil, plants and soil microbes are the three elements received considerable attention over several decades, of slope ecological environment, and an inseparable and the regulation and control mechanisms have been relationship exists among them. AMF served as a special partially determined [46, 66, 67]. Evidence has shown bond with them due to its improvement on soil structure that AMF could improve the uptake of P [4, 32], and properties [14, 32], plant development [46], and nitrogen [66], potassium [66], calcium, magnesium, microbial community [16], which strengthen the link and trace elements, and could contribute to about 70- between the three and then optimize slope environment. 80% of the P absorbed by hosts. There has been much speculation about the mechanism [46]: 1) mycelium Effects of AMF on Soil enlarges the absorption area of host roots [46]; 2) the content of organic acids in the root exudates increases As the terminologies used to describe the size and after inoculation with AMF to activate P in the soil arrangement of soil solids and pores, soil aggregates [68]; 3) the affinity between mycorrhizal and phosphate are strongly associated with soil porosity and water- is greater than that between non-mycorrhizal roots and holding capability [60]. Thirty-five experimental results phosphate, and the critical concentration of P absorption on AMF and soil aggregates have been synthesized and in hyphe is lower than that in root as well (Fig. 2); and finally confirmed the positive contribution of AMF to 4) the P transport rate in mycelia is faster than that the stabilization of soil aggregates [14]. The directly in plant roots [4]. And following the discovery of the enhancing mechanisms of AMF is through the release inducing effect of AMF on plant phosphate transporters, of intrahyphal components from mycorrhiza and the regulatory genes will have further information about the exudation and entanglement of hyphe and particles [60]. mechanism of AMF in promoting plant nutrition at the The intrahyphal components of filamentous AMF, the molecular level [57, 69]. most significant of which is the GRSP, would be released Studies have also shown that AMF has an effect during turnover [60], making the hyphal network sticky- on the secretion of plant hormones [34, 70]. AMF string bags, and stabilizing soil aggregates around them significantly increased the content of auxin, gibberellin, through bonding and entanglement. Furthermore, a and jasmonic acid in and roots of plants under recent experiment in New Caledonia showed that the normal and drought stress conditions [34, 70] and targeted screening of AMF could help the ecological decreased the contents of abscisic acid [70]. Increased restoration of bare slopes by their enhancement effect on hormone accumulation is associated with strigolactones soil aggregate stability [61], which further illustrates the secreted by plant roots and signal substances secreted by feasibility of AMF for slope restoration. mycelia, including sulfide oligosaccharides, non-sulfide AMF have been proven to affect soil properties, oligosaccharides and chitosan oligosaccharides [71]. include water content [62], particle size, soil pH, AMF can also promote the metabolism of polyamines electrical conductivity, and soil enzyme activities under stress and enhance plant tolerance through [63], through proliferation between or on the surface feedback regulation [72]. Moreover, the diversity and of soil particles as well [15]. The soil water retention colonization of AMF is in turn driven by the endogenous and hydraulic conductivity of AMF could help plants plant hormones levels [73], and such interactions adapt to variations in soil moisture [15]. Inoculation between AMF and phytohormone may result in positive with AMF would result in higher water availability due regulation of plant development. to the stronger water absorption of hypha and would make further efforts to restore the plant hydraulic status Interaction with Soil Microbes with higher soil drying rates [4, 33, 60]. Electrical conductivity, which has a positive correlation with soil The establishment of beneficial natural networks moisture within a certain range, has also been found between AMF and other beneficial soil microbes, which to have a clear correlation with AMF inoculation resulted from various symbiotic and nonsymbiotic [63, 64]. As for enzyme activities, though the impact associations, apparently evolved during plant growth mechanism is not yet clear, researchers have detected and development [4, 16, 17]. increases in β-glucosidase [63], catalase [45,63], urease A close relationship between symbiotic bacteria [17], dehydrogenase [17], protease [17], peroxidas and like rhizobium and AMF has been shown through dual dismutase [47], and phosphatase activities [17,63], inoculation experiments on plant yield, root colonization, and transient increases in catalase activity after AMF disease resistance [74], P content,[4] and nodule numbers inoculation [17]. Studies also have shown a negative [75]. Respiratory oxidative burst homolog-mediated correlation between AMF and clay content [64], which reactive oxygen species are considered to be vital may result in an increase in silt percentage. Those substances that play a critical role in this symbiosis [76]. results may be due to more oxygen provided by soil Apart from rhizobia, AMF also affects the symbiosis with a high sand content, which can satisfy the oxygen of plants and symbiotic actinomycetes, [4] though requirement of AMF [65]. sometimes antagonistic effects exist between these two 2036 Yan Y., et al. species, which may result in a detrimental effect on the by severe soil disturbances, but AMF on landward host [77]. slopes were not necessarily disturbance-sensitive – The interaction between AMF and non-symbiotic even if AMF abundance increased after disturbance bacteria in soil, especially P- solubilizing bacteria [82]. Kawahara et al. [82] indicated that the artificial [78], nitrobacteria and denitrobacteria [79], and some disturbance effects on the AMF community is due to autotrophic nitrogen-fixing bacteria [77], has been the emergence of hidden new members or a change in verified in numerous studies. A synergistic effect of the microbial abundance of the whole system, and AMF P-solubilizing bacteria and AMF in the improvement colonization on land slopes is interference-resistant to a of soil-neutral phosphatase activity and P uptake certain level. Besides, there is speculation that AMF can has been proved [78], which may be beneficial for quickly gain an advantage not only through the hyphal plant natural regeneration [78]. AMF abundance is network, but also through spores [82], which may be a positively correlated with the abundance of N2O- possible explanation for the advantage brought by AMF producing bacteria and is negatively correlated with the in the early stage while no mycorrhizal structure has abundance of N2O-consuming bacteria, so AMF can been formed. This is also the solution of giving artificial affect the structure of soil N-nutrition-related microbial AMF inoculum dominance in occupying the advantage populations [77]. Unlike the inhibition of ammonia- in the early recovery period so as to achieve the greatest oxidizing bacteria, soil nitrogen-fixing bacteria are potential. usually positively affected [4], which may be due to the nitrogen sources, of which the former originates from Existing Problems and Future Prospects the air while the latter is highly dependent on plant rhizosphere secretions [80]. Compared with laboratory research, practical Synergistic relationships were seen with AMF and difficulties are confronted with more challenges, which an epiphytic fungus in terms of mutual reinforcement can be summarized as follows: [4], which improved plant development and nutrient Restrictions on commercial AMF production. Due availability [4, 77]. Although the symbiotic relationship to the limitation of technology as well as costs, the between AMF and ecto-mycorrhizal fungi had also existing AMF production methods are only scratching been found [4, 48], this balance is not always positive, the surface of experimental needs, yet none of them and mutual inhibition was observed between them is actually satisfactory for both the quantity and [4]. Therefore, local microbes need to be carefully the quality demands of AMF inoculum required for considered for AMF application in different restoration restoration engineering [12]; 2) the storage method and conditioins in order to avoid negative effects in practical quality of AMF inoculum. As inoculum of endophytic application [2]. fungi, infected plant tissues must be used within their validity period to guarantee effectiveness. In addition to solid inoculum as the most widely used type [12, 83], Future Prospects for Applying AMF novel formulations applied in research, such as liquid in Slope Ecological Restoration inoculum, capsule inoculum and coating [12], which are restricted by the cost-factors in reality, are Relevant Applied Research difficult to successfully list. Many agent products on the market even usually rely on fertilizing compounds Significant achievements of laboratory and field added to them for the formation of mycorrhizal experiments on AMF technology suggest unlimited symbiosis, but poor-quality products hinder the potential to its application on SERT. However, this advancement of technology [81]; 3) The inoculation application has not been used generally. Therefore, method in engineering application. Pot culture is easy to the relationship between AMF and soil, plant, ensure the uniform mixing of AMF inoculum and microorganism in the disturbed area provides further for effective mycorrhizal symbiosis in experimental factual basis for feasibility. A project that validated the studies [34, 68], but this method is obviously not feasible feasibility of AMF for slope restoration was carried out for engineering because of the huge workload and the in the San Francisco River Basin, Brazil [81], which financial resource consumption [12]; and 4) Excellent explained the role of AMF species in disturbed slopes AMF effects generally occur in environmentally from the perspective of soil aggregation and stability. controlled experiments, yet in complex habitats of field This study also echoes the relationship between application, validity and efficiency are unstable, which AMF and soil stability from the perspective of slope is the maximum limit of putting mycorrhizal technology restoration. In addition, due to the particularity of the into practical application [12, 77]. Plant selectivity environment, the viability of AMF under engineering and interaction with soil microbes of AMF need to disturbance also calls for special emphasis to be summarized within the scope of pioneer plants in investigate its application as SERT materials. A study restoration engineering so that determining species aimed to evaluate the tolerance of AMF population arrangement may become easier [82, 83]. to soil disturbances found that the structure of plant Through analysis of the application environment, mycorrhizal communities on land slopes was affected advantages and limitations of the application potentiality, The Future Prospects of Arbuscular Mycorrhizal... 2037 the following practical and development directions and applying them in large-scale practical application of this technology are pointed out: 1) Close ties with are of great significance to technological innovation of production enterprises need to be established to form a slope ecological restoration. It is essential to thoroughly production chain for enlarging the production scale and research the interaction system among the microbes, increasing the production efficiency of AMF inoculum; plants and soil and the mechanisms involved, so that we 2) Related statutes and policies on the quality standard of can develop a new efficient method to attain satisfactory AMF inoculum needs be published to ensure the benefit results for slope ecological restoration. of better-quality products; 3) An artificial inoculation system needs to be established, such as stratified spraying and coat-pelleted seed technique [3, 8, 12], Acknowledgements which are applicable to slope engineering construction in order to reduce the economic losses caused by We acknowledge support from the National Key complex operation and develop a complete, rationally R&D Program of China (grant No. 2017YFC0504902) distributed maintenance management mode to guarantee and the National Natural Science Foundation of the sustainability; 4) The impacts of slope aspects and slope People’s Republic of China (grant No. 51678348). position on the AMF population require further study We thank LetPub (www.letpub.com) for its linguistic to indicate where optimization might be required for assistance during the preparation of this manuscript. construction on slopes; 5) The interaction mechanism between indigenous microorganisms and AMF is to be studied further to reduce the restrictions of mycorrhizal Conflict of Interest effect under uncontrolled complex environments; 6) More experimental data on host specificity of AMF The authors declare no conflict of interest. needs to be accumulated for a proprietary database of plants applied in slope ecological restoration in order to choose suitably engineered plants for a project [50]. 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